Functional cross-antagonism between transcription factors FLI-1 and EKLF

Molecular and Cellular Biology

Volumn 23, Issue 4, 2003, Pages 1390-1402

  Starck, Joëlle ^a   Cohet, Nathalie ^a   Gonnet, Colette ^a   Sarrazin, Sandrine ^a,e   Doubeikovskaia, Zina ^c   Doubeikovski, Alexandre ^d   Verger, Alexis ^b   Duterque Coquillaud, Martine ^b   Morle, François ^a  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^b CNRS   (France)

^c Inst Biochem Physiol M   (Russian Federation)

^d WEIS CENTER FOR RESEARCH   (United States)

^e CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLOBIN; COMPLEMENTARY DNA; ERYTHROID KRUPPEL LIKE FACTOR; GREEN FLUORESCENT PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR FLI 1; TRANSCRIPTION FACTOR GATA 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; DELETION MUTANT; DNA BINDING; ERYTHROCYTE; ERYTHROLEUKEMIA CELL; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; IMMUNOPRECIPITATION; MEGAKARYOCYTE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

ACETAMIDES; ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELLS, CULTURED; DNA; DNA-BINDING PROTEINS; ERYTHROCYTES; ERYTHROID-SPECIFIC DNA-BINDING FACTORS; GATA1 TRANSCRIPTION FACTOR; GLOBINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MOLECULAR SEQUENCE DATA; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; PROMOTER REGIONS (GENETICS); PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEIN C-FLI-1; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-ETS; RECOMBINANT PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

ANIMALIA;

EID: 0037312918     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.4.1390-1402.2003     Document Type: Article

References (80)

1. Afrikanova, I., E. Yeh, D. Bartos, S. S. Watowich, and G. D. Longmore. 2002. Oncogene cooperativity in Friend erythroleukemia: erythropoietin receptor activation by the env gene of SFFV leads to transcriptional upregulation of PU.1, independent of SFFV proviral insertion. Oncogene 21:1272-1284.
2. Athanasiou, M., P. A. Clausen, G. J. Mavrothalassitis, X. K. Zhang, D. K. Watson, and D. G. Blair. 1996. Increased expression of the ETS-related transcription factor FLI-1/ERGB correlates with and can induce the megakaryocytic phenotype. Cell Growth Differ. 7:1525-1534.
3. Athanasiou, M., G. Mavrothalassitis, L. Sun-Hoffman, and D. G. Blair. 2000. FLI-1 is a suppressor of erythroid differentiation in human hematopoietic cells. Leukemia 14:439-445.
4. Barnache, S., F. Wendling, C. Lacombe, N. Denis, M. Titeux, W. Vainchenker, and F. Moreau-Gachelin. 1998. Spi-1 transgenic mice develop a clonal erythroleukemia which does not depend on p53 mutation. Oncogene 16:2989-2995.
5. Barnache, S., P. Mayeux, B. Payrastre, and F. Moreau-Gachelin. 2001. Alterations of the phosphoinositide 3-kinase and mitogen-activated protein kinase signaling pathways in the erythropoietin-independent Spi-1/PU.1 transgenic proerythroblasts. Blood 98:2372-2381.
6. Bastian, L. S., M. Yagi, C. Chan, and G. J. Roth. 1996. Analysis of the megakaryocyte glycoprotein IX promoter identifies positive and negative regulatory domains and functional GATA and Ets sites. J. Biol. Chem. 271:18554-18560.
7. Bastian, L. S., B. A. Kwiatkowski, J. Breininger, S. Danner, and G. Roth. 1999. Regulation of the megakaryocytic glycoprotein IX promoter by the oncogenic Ets transcription factor Fil-1. Blood 93:2637-2644.
8. Ben-David, Y., and A. Bernstein. 1991. Friend virus-induced erythroleukemia and the multistage nature of cancer. Cell 66:831-834.
9. Bieker, J. J., and C. M. Southwood. 1995. The erythroid Kruppel-like factor transactivation domain is a critical component for cell-specific inducibility of a beta-globin promoter. Mol. Cell. Biol. 15:852-860.
10. Cantor, A. B., and S. H. Orkin. 2001. Hematopoietic development: a balancing act. Curr. Opin. Genet. Dev. 11:513-519.
11. Cantor, A. B., and S. H. Orkin. 2002. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene 21:3368-3376.
12. Carrere, S., A. Verger, A. Flourens, D. Stehelin, and M. Duterque-Coquillaud. 1998. Erg proteins, transcription factors of the Ets family, form homo, heterodimers and ternary complexes via two distinct domains. Oncogene 16:3261-3268.
13. Chen, X., and J. J. Bieker. 2001. Unanticipated repression function linked to erythroid Kruppel-like factor. Mol. Cell. Biol. 21:3118-3125.
14. Czuwara-Ladykowska, J., F. Shirasaki, P. Jackers, D. K. Watson, and M. Trojanowska. 2001. Fli-1 inhibits collagen type I production in dermal fibroblasts via an Sp1-dependent pathway. J. Biol. Chem. 276:20839-20848.
15. Darby, T. G., J. D. Meissner, A. Ruhlmann, W. H. Mueller, and R. J. Scheibe. 1997. Functional interference between retinoic acid of steroid hormone receptors and the oncoprotein Fli-1. Oncogene 15:3067-3082.
16. Debili, N., L. Coulombel, L. Croisille, A. Katz, J. Guichard, J. Breton-Gorius, and W. Vainchenker. 1996. Characterization of a bipotent erythromegakaryocytic progenitor in human bone marrow. Blood 88:1284-1296.
17. Delgado, M. D., P. Gutierrez, C. Richard, M. A. Cuadrado, F. Moreau-Gachelin, and J. Leon. 1998. Spi-1/PU.1 proto-oncogene induces opposite effects on monocytic and erythroid differentiation of K562 cells. Biochem. Biophys. Res. Commun. 252:383-391.
18. Deramaudt, T. B., P. Remy, and P. Stiegler. 2001. Identification of interaction partners for two closely-related members of the ETS protein family, FLI and ERG. Gene 274:169-177.
19. Deveaux, S., A. Filipe, V. Lemarchandel, J. Ghysdael, P. H. Romeo, and V. Mignotte. 1996. Analysis of the thrombopoietin receptor (MPL) promoter implicates GATA and Ets proteins in the coregulation of megakaryocyte-specific genes. Blood 87:4678-4785.
20. Doetzlhofer, A., H. Rotheneder, G. Lagger, M. Koranda, V. Kurtev, G. Brosch, E. Wintersberger, and C. Seiser. 1999. Histone deacetylase 1 can repress transcription by binding to Sp1. Mol. Cell. Biol. 19:5504-5511.
21. Donze, D., T. M. Townes, and J. J. Bieker. 1995. Role of erythroid Kruppel-like factor in human gamma- to beta-globin gene switching. J. Biol. Chem. 270:1955-1959.
22. Doubeikovskaia, Z., A. Aries, P. Jeannesson, F. Morle, and A. Doubeikovski. 2001. Purification of human recombinant GATA-1 from bacteria: implication for protein-protein interaction studies. Protein Expr. Purif. 23:426-431.
23. Eisbacher, M., L. M. Khachigian, T. H. Khin, M. L. Holmes, and B. H. Chong. 2001. Inducible expression of the megakaryocyte-specific gene glycoprotein IX is mediated through an Ets binding site and involves upstream activation of extracellular signal-regulated kinase. Cell Growth Differ. 12:435-445.
24. Gregory, R. C., D. J. Taxman, D. Seshasayee, M. H. Kensinger, J. J. Bieker, and D. M. Wojchowski. 1996. Functional interaction of GATA1 with crythroid Kruppel-like factor and Sp1 at defined erythroid promoters. Blood 87:1793-1801.
25. Gutman, A., and B. Wasylyk. 1990. The collagenase gene promoter contains a TPA and oncogene-responsive unit encompassing the PEA3 and AP-1 binding sites. EMBO J. 9:2241-2246.
26. Hallier, M., A. Tavitian, and F. Moreau-Gachelin. 1996. The transcription factor Spi-1/PU.1 binds RNA and interferes with the RNA-binding protein p54nrb. J. Biol. Chem. 271:11177-11181.
27. Hallier, M., A. Lerga, S. Barnache, A. Tavitian, and F. Moreau-Gachelin. 1998. The transcription factor Spi-1/PU.1 interacts with the potential splicing factor TLS. J. Biol. Chem. 273:4838-4842.
28. Hart, A., F. Melet, P. Grossfeld, K. Chien, C. Jones, A. Tunnacliffe, R. Favier, and A. Bernstein. 2000. Fli-1 is required for murine vascular and megakaryocytic development and is hemizygously deleted in patients with thrombocytopenia. Immunity 13:167-177.
29. Hong, W., A. Y. Kim, S. Ky, C. Rakowski, S. B. Deo, D. Chakravarti, M. Atchison, and G. A. Blobel. 2002. Inhibition of CBP-mediated protein acetylation by the Ets family oncoprotein PU.1. Mol. Cell. Biol. 22:3729-3743.
30. Jaishankar, S., J. Zhang, M. F. Roussel, and S. J. Baker. 1999. Transforming activity of EWS/FLI is not strictly dependent upon DNA-binding activity. Oncogene 18:5592-5597.
31. Kawada, H., T. Ito, P. N. Pharr, D. D. Spyropoulos, D. K. Watson, and M. Ogawa. 2001. Defective megakaryopoiesis and abnormal erythroid development in Fli-1 gene-targeted mice. Int. J. Hematol. 73:463-468.
32. Kihara-Negishi, F., H. Yamamoto, M. Suzuki, T. Yamada, T. Sakurai, T. Tamura, and T. Oikawa. 2001. In vivo complex formation of PU.1 with HDAC1 associated with PU.1-mediated transcriptional repression. Oncogene 20:6039-6047.
33. Knoop, L. L., and S. J. Baker. 2001. EWS/FLI alters 5′-splice site selection. J. Biol. Chem. 276:22317-22322.
34. Latchman, D. S. 2001. Transcription factors: bound to activate or repress. Trends Biochem. Sci. 26:211-213.
35. Lemercier, C., A. Verdel, B. Galloo, S. Curtet, M. P. Brocard, and S. Khochbin. 2000. mHDA1/HDAC5 histone deacetylase interacts with and represses MEF2A transcriptional activity. J. Biol. Chem. 275:15594-15599.
36. Lesault, I., C. T. Quang, J. Frampton, and J. Ghysdael. 2002. Direct regulation of BCL-2 by FLI-1 is involved in the survival of FLI-1-transformed erythroblasts. EMBO J. 21:694-703.
37. Lim, S. K., J. J. Bieker, C. S. Lin, and F. Costantini. 1997. A shortened life span of EKLF-/- adult erythrocytes, due to a deficiency of beta-globin chains, is ameliorated by human gamma-globin chains. Blood 90:1291-1299.
38. Littlewood, T. D., D. C. Hancock, P. S. Danielian, M. G. Parker, and G. I. Evan. 1995. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 23:1686-1690.
39. Martin, D. I., and S. H. Orkin. 1990. Transcriptional activation and DNA binding by the erythroid factor GF-1/NF-E1/Eryf 1. Genes Dev. 4:1886-1898.
40. Matsumura, I., A. Kawasaki, H. Tanaka, J. Sonoyama, S. Ezoe, N. Minegishi, K. Nakajima, M. Yamamoto, and Y. Kanakura. 2000. Biologic significance of GATA-1 activities in Ras-mediated megakaryocytic differentiation of hematopoietic cell lines. Blood 96:2440-2450.
41. Melet, F., B. Motro, D. J. Rossi, L. Zhang, and A. Bernstein. 1996. Generation of a novel Fli-1 protein by gene targeting leads to a defect in thymus development and a delay in Friend virus-induced erythroleukemia. Mol. Cell. Biol. 16:2708-2718.
42. Melot, T., N. Gruel, A. Doubeikovski, N. Sevenet, T. L. Teillaud, and O. Delattre. 1997. Production and characterization of mouse monoclonal antibodies to wild-type and oncogenic FLI-1 proteins. Hybridoma 16:457-464.
43. Miller, I. J., and J. J. Bieker. 1993. A novel, erythroid cell-specific murine transcription factor that binds to the CACCC element and is related to the Kruppel family of nuclear proteins. Mol. Cell. Biol. 13:2776-2786.
44. Moreau-Gachelin, F., F. Wendling, T. Molina, N. Denis, M. Titeux, G. Grimber, P. Briand, W. Vainchenker, and A. Tavitian. 1996. Spi-1/PU.1 transgenic mice develop multistep erythroleukemias. Mol. Cell. Biol. 16:2453-2463.
45. Moreau-Gachelin, F., A. Tavitian, and P. Tambourin. 1988. Spi-1 is a putative oncogene in virally induced murine erythroleukaemias. Nature 331:277-280.
46. Nerlov, C., E. Querfurth, H. Kulessa, and T. Graf. 2000. GATA-1 interacts with the myeloid PU.1 transcription factor and represses PU.1-dependent transcription. Blood 95:2543-2551.
47. Oikawa, T., T. Yamada, F. Kihara-Negishi, H. Yamamoto, N. Kondoh, Y. Hitomi, and Y. Hashimoto. 1999. The role of Ets family transcription factor PU.1 in hematopoietic cell differentiation, proliferation and apoptosis. Cell Death Differ. 6:599-608.
48. Orkin, S. H. 2000, Diversification of haematopoietic stem cells to specific lineages. Nat. Rev. Genet. 1:57-64.
49. Ozawa, Y., M. Towatari, S. Tsuzuki, F. Hayakawa, T. Maeda, Y. Miyata, M. Tanimoto, and H. Saito. 2001. Histone deacetylase 3 associates with and represses the transcription factor GATA-2. Blood 98:2116-2123.
50. Pandya, K., D. Donze, and T. M. Townes. 2001. Novel transactivation domain in erythroid Kruppel-like factor (EKLF). J. Biol. Chem. 276:8239-8243.
51. Pereira, R., C. T. Quang, I. Lesault, H. Dolznig, H. Beug, and J. Ghysdael. 1999. FLI-1 inhibits differentiation and induces proliferation of primary erythroblasts. Oncogene 18:1597-1608.
52. Pereira, R., J. Raingeaud, M. Pironin, J. Ghysdael, and C. T. Quang. 2000. SPI-1 transforming properties depend upon specifically activated forms of the EPOR. Oncogene 19:5106-5110.
53. Quang, C. T., O. Wessely, M. Pironin, H. Beug, and J. Ghysdael. 1997. Cooperation of Spi-1/PU.1 with an activated erythropoietin receptor inhibits apoptosis and Epo-dependent differentiation in primary erythroblasts and induces their Kit ligand-dependent proliferation. EMBO J. 16:5639-5653.
54. Rao, G., N. Rekhtman, G. Cheng, T. Krasikov, and A. I. Skoultchi. 1997. Deregulated expression of the PU.1 transcription factor blocks murine erythroleukemia cell terminal differentiation. Oncogene 14:123-131.
55. Rekhtman, N., F. Radparvar, T. Evans, and A. I. Skoultchi. 1999. Direct interaction of hematopoietic transcription factors PU.1 and GATA-1: functional antagonism in erythroid cells. Genes Dev. 13:1398-1411.
56. Sarrazin, S., J. Starck, C. Gonnet, A. Doubeikovski, F. Melet, and F. Morle. 2000, Negative and translation termination-dependent positive control of FLI-1 protein synthesis by conserved overlapping 5′ upstream open reading frames in Fli-1 mRNA. Mol. Cell. Biol. 20:2959-2969.
57. Scully, K. M., E. M. Jacobson, K. Jepsen, V. Lunyak, H. Viadiu, C. Carriere, D. W. Rose, F. Hooshmand, A. K. Aggarwal, and M. G. Rosenfeld. 2000. Allosteric effects of Pit-1 DNA sites on long-term repression in cell type specification. Science 290:1127-1131.
58. Shivdasani, R. A. 2001. Molecular and transcriptional regulation of megakaryocyte differentiation. Stem Cells 19:397-407.
59. Sieweke, M. H., and T. Graf. 1998. A transcription factor party during blood cell differentiation. Curr. Opin. Genet. Dev. 8:545-551.
60. Simon, M. C. 1998. PU.1 and hematopoiesis: lessons learned from gene targeting experiments. Semin. Immunol. 10:111-118.
61. Singh, H., R. P. DeKoter, and J. C. Walsh. 1999. PU.1, a shared transcriptional regulator of lymphoid and myeloid cell fates. Cold Spring Harb. Symp. Quant. Biol. 64:13-20.
62. Spyropoulos, D. D., P. N. Pharr, K. R. Lavenburg, P. Jackers, T. S. Papas, M. Ogawa, and D. K. Watson. 2000. Hemorrhage, impaired hematopoiesis, and lethality in mouse embryos carrying a targeted disruption of the Fli1 transcription factor. Mol. Cell. Biol. 20:5643-5652.
63. Starck, J., A. Doubeikovski, S. Sarrazin, C. Gonnet, G. Rao, A. Skoultchi, J. Godet, I. Dusanter-Fourt, and F. Morle. 1999. Spi-1/PU.1 is a positive regulator of the Fli-1 gene involved in inhibition of erythroid differentiation in friend erythroleukemic cell lines. Mol. Cell. Biol. 19:121-135.
64. Starck, J., G. Mouchiroud, C. Gonnet, A. Mehlen, D. Aubert, A. Dorier, J. Godet, and F. Morle. 1999. Unexpected and coordinated expression of Spi-1, Fli-1, and megakaryocytic genes in four Epo-dependent cell lines established from transgenic mice displaying erythroid-specific expression of a thermosensitive SV40 T antigen. Exp. Hematol. 27:630-641.
65. Sugihara, T. M., E. I. Kudryavtseva, V. Kumar, J. J. Horridge, and B. Andersen. 2001. The POU domain factor Skin-1a represses the keratin 14 promoter independent of DNA binding. A possible role for interactions between Skn-1a and CREB-binding protein/p300. J. Biol. Chem. 276:33036-33044.
66. Tamir, A., J. Howard, R. R. Higgins, Y. J. Li, L. Berger, E. Zacksenhaus, M. Reis, and Y. Ben-David. 1999. Fli-1, an Ets-related transcription factor, regulates erythropoietin-induced erythroid proliferation and differentiation: evidence for direct transcriptional repression of the Rb gene during differentiation. Mol. Cell. Biol. 19:4452-4464.
67. Tewari, R., N. Gillemans, M. Wijgerde, B. Nuez, M. von Lindern, F. Grosveld, and S. Philipsen. 1998. Erythroid Kruppel-like factor (EKLF) is active in primitive and definitive erythroid cells and is required for the function of 5′HS3 of the beta-globin locus control region. EMBO J. 17:2334-2341.
68. Truong, A. H., and Y. Ben-David. 2000. The role of Fli-1 in normal cell function and malignant transformation. Oncogene 19:6482-6489.
69. Yamada, T., N. Kondoh., M. Matsumoto, M. Yoshida, A. Maekawa, and T. Oikawa. 1997. Overexpression of PU.1 induces growth and differentiation inhibition and apoptotic cell death in murine erythroleukemia cells. Blood 89:1383-1393.
70. Yamada, T., F. Kihara-Negishi, H. Yamamoto, M. Yamamoto, Y. Hashimoto, and T. Oikawa. 1998. Reduction of DNA binding activity of the GATA-1 transcription factor in the apoptotic process induced by overexpression of PU.1 in murine erythroleukemia cells. Exp. Cell Res. 245:186-194.
71. Yamamoto, H., F. Kihara-Negishi, T. Yamada, Y. Hashimoto, and T. Oikawa. 1999. Physical and functional interactions between the transcription factor PU.1 and the coactivator CBP. Oncogene 18:1495-1501.
72. Yamamoto, H., F. Kihara-Negishi, T. Yamada, M. Suzuki, T. Nakano, and T. Oikawa. 2002. Interaction between the hematopoietic Ets transcription factor Spi-B and the coactivator CREB-binding protein associated with negative cross-talk with c-Myb. Cell Growth Differ. 13:69-75.
73. Yang, S. H., E. Vickers, A. Brehm, T. Kouzarides, and A. D. Sharrocks. 2001. Temporal recruitment of the mSin3A-histone deacetylase corepressor complex to the ETS domain transcription factor Elk-1. Mol. Cell. Biol. 21:2802-2814.
74. Yao, Y. L., W. M. Yang, and E. Seto. 2001. Regulation of transcription factor YY1 by acetylation and deacetylation. Mol. Cell. Biol. 21:5979-5991.
75. Yi, H., Y. Fujimura, M. Ouchida, D. D. Prasad, V. N. Rao, and E. S. Reddy. 1997. Inhibition of apoptosis by normal and aberrant Fli-1 and erg proteins involved in human solid tumors and leukemias. Oncogene 14:1259-1268.
76. Zhang, L., A. Eddy, Y. T. Teng, M. Fritzler, M. Kluppel, F. Melet, and A. Bernstein. 1995. An immunological renal disease in transgenic mice that overexpress Fli-1, a member of the ets family of transcription factor genes. Mol. Cell. Biol. 15:6961-6970.
77. Zhang, P., G. Behre, J. Pan, A. Iwama, N. Wara-Aswapati, H. S. Radomska, P. E. Auron, D. G. Tenen, and Z. Sun. 1999. Negative cross-talk between hematopoietic regulators: GATA proteins repress PU.1. Proc. Natl. Acad. Sci. USA 96:8705-8710.
78. Zhang, P., X. Zhang, A. Iwama, C. Yu, K. A. Smith, B. U. Mueller, S. Narravula, B. E. Torbett, S. H. Orkin, and D. G. Tenen. 2000. PU.1 inhibits GATA-1 function and erythroid differentiation by blocking GATA-1 DNA binding. Blood 96:2641-2648.
79. Zhang, W., S. Kadam, B. M. Emerson, and J. J. Bieker. 2001. Site-specific acetylation by p300 or CREB binding protein regulates erythroid Kruppel-like factor transcriptional activity via its interaction with the SWI-SNF complex. Mol. Cell. Biol. 21:2413-2422.
80. Zochodne, B., A. H. Truong, K. Stetler, R. R. Higgins, J. Howard, D. Dumont, S. A. Berger, and Y. Ben-David. 2000. Epo regulates erythroid proliferation and differentiation through distinct signaling pathways: implication for erythropoiesis and Friend virus-induced erythroleukemia. Oncogene 19:2296-2304.